Rickettsiae in red fox (Vulpes vulpes), marbled polecat (Vormela peregusna) and their ticks in northwestern China

Wurelihazi Hazihan,Ligu Mi,Shanshan Zhao,Zhiqiang Liu,Xinli Gu,Wumei Yuan,Sándor Hornok,Yanyan Zhang,Gang Liu,Yuanzhi Wang,Suwen Wang,Wenbo Tan

doi:10.1186/s13071-021-04718-1

Abstract

BackgroundPreviously, twelve Rickettsia species were identified in ticks, fleas, sheep keds (Melophagus ovinus), bats (Pipistrellus pipistrellus) and a tick-bitten patient in the Xinjiang Uygur Autonomous Region (XUAR) in northwestern China. Here we aimed to molecularly detect rickettsial agents in red fox (Vulpes vulpes), marbled polecat (Vormela peregusna) and their ticks.MethodsDuring 2018–2019, 12 red foxes, one marbled polecat and their ticks were sampled in two counties and a city of the XUAR. The heart, liver, spleen, lung and kidney of these 13 carnivores were dissected, followed by DNA extraction. Hard ticks were identified both morphologically and molecularly. All samples were examined for the presence of rickettsiae by amplifying four genetic markers (17-kDa, gltA, ompA, sca1).ResultsA total of 26 adult ticks and 28 nymphs (38 Ixodes canisuga, nine Ixodes kaiseri, six Haemaphysalis erinacei and one Dermacentor marginatus) were collected from red foxes, and four Ha. erinacei ticks were removed from the marbled polecat. Analysis of cytochrome c oxidase subunit I (COI) gene sequences indicated that 2–32 nucleotides differed between I. canisuga, I. kaiseri and Ha. erinacei from northwestern China and Europe. Rickettsia raoultii was detected in three red foxes, Candidatus Rickettsia barbariae in a red fox, Rickettsia sibirica in a red fox and a marbled polecat, and R. raoultii in two tick species (I. canisuga and D. marginatus).ConclusionsTo the best of our knowledge, I. canisuga and I. kaiseri have not been previously reported from red foxes in China. The DNA of R. sibirica and R. raoultii was detected for the first time in the organs of red foxes, and R. sibirica in the organs of a marbled polecat. This is also the first molecular evidence for the presence of R. raoultii in I. canisuga. Our findings expand the range of tick-borne pathogens in wildlife species and associated ticks in China.Graphical

Highlights

Twelve Rickettsia species were identified in ticks, fleas, sheep keds (Melophagus ovinus), bats (Pipistrellus pipistrellus) and a tick-bitten patient in the Xinjiang Uygur Autonomous Region (XUAR) in northwestern China
Tick identification A total of 26 adult ticks and 28 nymphs (i.e., 38 I. canisuga, 9 I. kaiseri, 6 Ha. erinacei and 1 D. marginatus) were collected from 12 red foxes, and four Ha. erinacei ticks were found on the marbled polecat
(“A to K”) [17] (Fig. 1a); (ii) I. kaiseri from red foxes in the XUAR was in basal position to nine European haplotypes (“L to T”), and had an identical sequence with conspecific ticks from long-tailed ground squirrels and Asian badgers [17, 30, 33] (Fig. 1b); (iii) Ha. erinacei from red foxes and marbled polecat had identical sequences, and formed a distinct clade from those reported in Turkey, Italy and Romania (Fig. 1c); and (iv) D. marginatus from red fox #2 had an identical sequence with the off-host tick collected formerly in Altaw City, XUAR

Summary

Introduction

Twelve Rickettsia species were identified in ticks, fleas, sheep keds (Melophagus ovinus), bats (Pipistrellus pipistrellus) and a tick-bitten patient in the Xinjiang Uygur Autonomous Region (XUAR) in northwestern China. We aimed to molecularly detect rickettsial agents in red fox (Vulpes vulpes), marbled polecat (Vormela peregusna) and their ticks. Red foxes were reported to harbor several vector-borne pathogens of public health concern, including tick-borne encephalitis virus [3], Borrelia burgdorferi [4], Ehrlichia canis [5], Leishmania infantum [6], Hepatozoon canis [7] and Babesia vulpes [8, 9]. The geographic range of the marbled polecat (Vormela peregusna) covers Central Asia, northwestern China and Europe [2]. In studies on its epidemiological role, seroconversion to plague F1 antigen was detected in a marbled polecat in the Xinjiang Uygur Autonomous Region (XUAR) [11] in northwestern China. R. raoultii and Candidatus Rickettsia barbariae were molecularly identified in marbled polecats in the XUAR [13]

Objectives

Methods

Results

Discussion

Conclusion